Data were retrieved from 7 of 14 devices implanted in wild Minnesota black bears (Ursus americanus
), and also from a bear that was kept in captivity over winter and released in spring. Annual HR and activity data were successfully retrieved from 6 bears and partial data sets were retrieved from 2 bears shot by hunters in the fall. The data from the other 7 devices were lost when bears were shot by hunters and not retrieved or when rejected by bears due to a foreign body response (as has been previously reported for other devices implanted in wild bears) [7
]. The devices that remained implanted showed no evidence of inflammation or irritation. All sutures had been absorbed and the subcutaneous insertion sites (an incision of 1.5 cm) were no longer detectable. For the devices that were rejected, the implantation site was no longer detectable and could only be located via the patch of hair that had been shaved at the time of implant. The animals from which annual datasets were successfully collected included: two adult males, two females with cubs that denned with them during the subsequent winter as yearlings, a female with yearlings that became pregnant and gave birth to two cubs during the winter study period, and a female for which two consecutive years of data were obtained, who denned with yearlings during one winter and gave birth to cubs the second year.
Extremes in average daytime HR (08:00-20:00) ranged from 8 beats/minute (bpm) in the winter (during hibernation) to 135 bpm in the summer, with nighttime (0:00-04:00) averages of 7 to 139 bpm (i.e., similar ranges in daily averages for day and night). During the period of captivity, bear 5 had a maximum daytime average heart rate of 144 bpm and a maximum nighttime average heart rate of 150 bpm. These data were not included in the range reported above due to the unnatural conditions. The longest period of asystole confirmed with an ECG was 14.4 seconds in bear 3 during a period where the respiration rate was 1.53 breaths/minute (winter; equivalent heart rate of 4 bpm) and the maximum HR confirmed with an ECG was 214 bpm (summer). ICMs recorded an average of 25.0 ± 1.6 million heart beats/year for the bears (Range: 23.3 - 27.4 million beats/year). Activity sensors documented a minimum of 0 minutes (winter) to a maximum of 1084 minutes (summer) of activity over a 24 hour period. See Table .
Summary of heart rate and activity data recorded over a 12 month period in wild black bears.
Trends and levels of HR and activity (time active per day) were similar for the six animals with complete data sets (representative examples shown in Figures , and ). Both HR and activity increased through the spring for at least a month following emergence from hibernation in early April. Activity then reached a generally steady state for several months, whereas HRs continued to increase over the summer months. During the spring and summer months the population of bears was more diurnal, as indicated by the statistically higher daytime HRs for the months of March-August, and generally more nocturnal in the months of September and October. Although nocturnal activity did not achieve significance for the population in any single month, nighttime HR was significantly higher at least once in 5 of 6 bears in September and/or October (excludes bears shot by hunters in the fall; detailed in Table ).
Figure 1 Twelve month heart rate and activity data for Bear 1 (female denning with cubs in 2009 and yearlings in 2010) and Bear 2 (female denning with yearlings in 2009 and giving birth to cubs in 2010). Average daytime heart rate (blue; 08:00-20:00), average (more ...)
Figure 2 Twelve month heart rate and activity data for two consecutive years from Bear 3 (#2213; female denning with cubs in 2009 and yearlings in 2010, and giving birth to cubs in 2011). Average daytime heart rate (blue; 08:00-20:00), average nightly heart rate (more ...)
Figure 3 Twelve month heart rate and activity data for Bear 4 (#R4041; male) and Bear 5 (#2123; male shot by hunter). Average daytime heart rate (blue; 08:00-20:00), average nightly heart rate (red; 0:00-04:00 AM), and daily activity (black line) are shown. Initiation (more ...)
A sharp decline in both HR and activity occurred in September and October, with the first day of denning evident from a dramatic drop in activity (Figures , and ). The duration of winter inactivity (including 2 winters for bear 3) was 176 ± 20 days (range: 148 to 195 days) with only 24 ± 6% of heart beats occurring during this period. A sharp increase in heart rate was evident in late December for all bears, corresponding to the winter den visit by the research team; this elevated rate was sustained for 1-2 days after our disturbance. During our March visit to the den of the female with newborn cubs (bear 2), there were fresh wolf tracks near the den entrance. This encounter resulted in only a subtle increase in activity and heart rate, as there were no large spikes in the record. A sharp cessation of activity in mid-January preceded by a period of elevated heart rate is seen in the expanded plot for bear 2 (Figure ) and in the second year for bear 3, corresponding to the birth of cubs. The mother may have remained in a more stationary position immediately after birthing so as not to crush the altricial cubs, which stay warm underneath her, and to provide them constant access to milk. Changes in mid-winter activity were not observed for the females with yearlings (which do not nurse during winter). The ICM in bear 4 (an adult male) ceased collecting activity data in early June during the height of the breeding season. The cause of the data loss is not yet known because the device remains implanted, but we suspect that the activity circuitry may have been damaged since cessation of data collection correlated to a period of high heart rate and activity. The device lies just under the skin, so is potentially vulnerable to damage from high impact.
The trend data for one of two bears legally shot by a hunter is shown in the lower panel of Figure (bear 5). The general trends in heart rate and activity are similar to bears 1-4 with the exception of the late winter/springtime data during which time this bear was housed outdoors in a wildlife rescue facility. Although the activity levels (physical movement) of bear 5 were very limited and appeared to be similar to the other bears in late hibernation, the bear's heart rate was substantially elevated until it was released into the wild (May 7). The data from bear 5 were included here because they demonstrate the physiological reaction to the hunt and also highlight the disparity in heart rates between captive and free-ranging bears.
A unique feature of the ICM is the automatic generation of HR plots and the recording of ECGs during triggered events. The plots compare the interval between consecutive heart beats in milliseconds on the abscissa (1000 msec interval corresponding to a HR of 60 bpm) to time in seconds on the ordinate axis. The plots were truncated by the ICM at an interval of 1500 msec since such slow rates were not anticipated in human clinical use. Examples of HR plots recording during the team's approach to the den site of bear 1 are shown in Figure . A slow HR and respiration rate, with a pronounced respiratory sinus arrhythmia (RSA) was present at 07:35 prior to the team's arrival. Upon our approach to the den at 09:36 both the HR and respiration rate accelerated, even though we made a concerted attempt to be very quiet. The accelerated HR and respiration continued, with a dampening of the RSA following administration of the immobilizing drugs but prior to the bear being fully anesthetized. A stable rate of approximately 120 bpm with no RSA occurred under the full effect of the anesthetic agent. This series was typical of the bears studied and demonstrates the alertness of the bear while in a state of hibernation to potential dangers outside the den. Such physiological responses were not always apparent through simply observing the behavior and activity of the bear in the den.
Figure 4 Heart rate changes in a wild bear during a visit to the den site. Sequences automatically recorded on 17-Dec-09 during a visit to the den of bear 1. Panels show heart rate trends: prior to arrival at the den (slow heart rate with RSA), after arrival (team (more ...)
Extremes in HR are demonstrated in Figures . Examples are shown for two bears that survived the entire year, including both the HR trend plot and an embedded ECG correlating to the period of maximum HR. A heart rate of 214 bpm was confirmed from the ECG trace for bear 1. The upper panel in the figure demonstrates a HR acceleration from a stable heart rate of approximately 85 bpm to a rate of over 200 bpm. The lower panel demonstrates a HR acceleration from a period with a pronounced RSA. The acceleration to a rate of 176 bpm appears to be associated with an exaggerated respiratory cycle. The presence of the RSA is evidenced by the oscillations in the HR and can be confirmed by modulations in the ECG amplitudes detected by the ICM. This amplitude modulation is a result of variations in intra-body impedances during chest expansions and lung inflations [25
]. From analysis of these oscillations on the embedded ECG on the lower panel of Figure , the respiration rate of bear 3 was found to average 4 breaths/minute. HR cycle lengths of less than 200 msec were recorded in other episode plots (300 bpm equivalent) but were always associated with oversensing of T-waves by the ICM. Only the maximum and minimum values that could be confirmed with ECGs were reported to eliminate the possibility of erroneous rhythm interpretation by the device.
Figure 5 Elevated heart rates recorded from two free-ranging wild black bears. The top panel demonstrates heart rate acceleration from a steady rate of approximately 85 bpm to 214 bpm. The bottom panels shows an acceleration during a period with a pronounced respiratory (more ...)
The highest heart rate documented during this study was from an animal that was legally shot during the fall hunting season (bear 5; Figure ). Although this bear was not detected by the hunter's trail camera at his bait site until just before it was shot, the bear's HR exceeded 200 bpm for 17 episodes in the 3 hours prior to being shot, suggesting that the bear was in the area of the hunter's bait and sensed danger. The final recordings from this bear included an interval with an average heart rate of 251 bpm, with a minimum interval between consecutive heart beats of 210 milliseconds (corresponds to an instantaneous heart rate of 285 bpm; see the upper right panel in Figure ). The final recordings for the second bear shot by a hunter (bear 6) indicated an average HR of 200 bpm sustained for 64 seconds with a peak of 207 bpm.
Figure 6 ECG trends from a hunted bear. Sequences automatically recorded from 16:43 - 16:59 on 02-Sep-10 during the time period when bear 6 was legally shot and killed by a hunter. This device was returned to the research team by the hunter. Panels show heart (more ...)
The longest period of asystole confirmed with an ECG trace is plotted in Figure . Bear 3 had three consecutive respiratory cycles documented with ECG recordings, and showed sinus pauses of 14.4, 14.3, and 13.7 seconds. The average respiratory rate during this period was 1.53 breaths/minute (3 breaths in 117.6 seconds). The morphology of the ECG was similar before and after the pause, indicating that it is a natural heart beat emanating from the sinoatrial node. All animals filled the available device memory for asystolic events, with 65,565 sinus pauses of at least 4.5 seconds documented.
Figure 7 Heart rate intervals for three consecutive respiratory cycles from a free-ranging wild black bear. The heart rate intervals for 34 consecutive beats were recorded on 18-Dec-09 at 12:20 PM for bear 3 (#2213). The ECG inset in the figure corresponds to (more ...)
The cumulative heart rate and activity results are summarized in Figure . All data were included in this analysis, with the exception of the data related to the period of captivity for bear 5. As expected, a dramatic decrease in heart rate and activity are evident during the winter months. Although a statistically significant shift to nocturnal behavior in the fall was seen when comparing the average daytime and nighttime heart rates for each month for individual bears, the difference was not significant for any single month when viewed across the population.
Figure 8 Annual trends in heart rate and activity in free-ranging wild black bears. The average daytime heart rate, nighttime heart rate, and daily activity are plotted (two years are included for bear 3). The error bar indicates one standard deviation. The sample (more ...)